Molecular characterization of the SPL gene family in Populus trichocarpa
© Li and Lu; licensee BioMed Central Ltd. 2014
Received: 30 March 2014
Accepted: 6 May 2014
Published: 15 May 2014
SPLs, a family of transcription factors specific to plants, play vital roles in plant growth and development through regulation of various physiological and biochemical processes. Although Populus trichocarpa is a model forest tree, the PtSPL gene family has not been systematically studied.
Here we report the identification of 28 full-length PtSPLs, which distribute on 14 P. trichocarpa chromosomes. Based on the phylogenetic relationships of SPLs in P. trichocarpa and Arabidopsis, plant SPLs can be classified into 6 groups. Each group contains at least a PtSPL and an AtSPL. The N-terminal zinc finger 1 (Zn1) of SBP domain in group 6 SPLs has four cysteine residues (CCCC-type), while Zn1 of SPLs in the other groups mainly contains three cysteine and one histidine residues (C2HC-type). Comparative analyses of gene structures, conserved motifs and expression patterns of PtSPLs and AtSPLs revealed the conservation of plant SPLs within a group, whereas among groups, the P. trichocarpa and Arabidopsis SPLs were significantly different. Various conserved motifs were identified in PtSPLs but not found in AtSPLs, suggesting the diversity of plant SPLs. A total of 11 pairs of intrachromosome-duplicated PtSPLs were identified, suggesting the importance of gene duplication in SPL gene expansion in P. trichocarpa. In addition, 18 of the 28 PtSPLs, belonging to G1, G2 and G5, were found to be targets of miR156. Consistently, all of the AtSPLs in these groups are regulated by miR156. It suggests the conservation of miR156-mediated posttranscriptional regulation in plants.
A total of 28 full-length SPLs were identified from the whole genome sequence of P. trichocarpa. Through comprehensive analyses of gene structures, phylogenetic relationships, chromosomal locations, conserved motifs, expression patterns and miR156-mediated posttranscriptional regulation, the PtSPL gene family was characterized. Our results provide useful information for evolution and biological function of plant SPLs.
SPL proteins constitute a diverse family of transcription factors playing vital roles in plant growth and development. SPLs are specific to plants and have a highly conserved SBP (SQUAMOSA PROMOTER BINDING PROTEIN) domain with approximately 78 amino acid residues. The domain contains three functionally important motifs, including zinc finger 1 (Zn1), zinc finger 2 (Zn2), and nuclear location signal (NLS) [1, 2]. Genes encoding SPLs were first identified for SBP1 and SBP2 in Antirrhinum majus. Lately, it has been found in various green plants, including single-celled green algae, mosses, gymnosperms, and angiosperms. The results showed that SPLs existed as a large gene family in plants. For instance, the SPL gene family in Arabidopsis, rice, Physcomitrella patens, maize and tomato includes 16, 19, 13, 31 and 15 members, respectively [4–9].
The 16 Arabidopsis SPLs are termed as AtSPL1 to AtSPL16, respectively, of which AtSPL1, AtSPL7, AtSPL12, AtSPL14 and AtSPL16 are relatively large and expressed constitutively, while the others are relatively small and highly expressed in flowers [4, 10]. Ten of the 16 AtSPLs, including AtSPL2–AtSPL6, AtSPL9–AtSPL11, AtSPL13 and AtSPL15, are regulated by miRNAs belonging to the MIR156 family [11–17]. AtSPL3, AtSPL4 and AtSPL5 contain complementary sequences of miR156 in 3’ UTR, and all of them promote vegetative phase change and flowering [10, 14, 18]. AtSPL2, AtSPL10 and AtSPL11 regulate morphological traits of cauline leaves and flowers . Overexpression of miR156b reduces the accumulation of AtSPL2, AtSPL10 and AtSPL11 mRNA [12, 14, 20]. AtSPL9 and AtSPL15 act redundantly in controlling the juvenile-to-adult growth phase transition and leaf initiation rate in Arabidopsis. Six AtSPLs, including AtSPL1, AtSPL7, AtSPL8, AtSPL12, AtSPL14 and AtSPL16, are not targets of miR156 in Arabidopsis. Among them, AtSPL7 can bind directly to the Cu-response element (CuRE) containing a core sequence of GTAC and is a regulator of Cu homeostasis in Arabidopsis. AtSPL8 regulates pollen sac development , male fertility , GA biosynthesis and signaling . AtSPL14 plays significant roles in plant development and sensitivity to fumonisin B1 . Among the 19 rice SPLs, half are predominantly expressed in various young organs . OsSPLs targeted by miR156 are involved in the development of flowers in rice. OsSPL14 regulated by miR156 also controls shoot branching in the vegetative stage [8, 28, 29]. In maize, liguleless1containing the SBP domain regulates ligule and auricle formation [30, 31].
Populus trichocarpa is a model plant with whole genome sequence available . A total of 352 miRNA precursors, including 12 for miR156, have been identified [33–39]. However, the regulation of miR156 in P. trichocarpa PtSPLs has not been analyzed. In our previous studies , 17 PtSPLs, which appeared to be full-length or partial sequence with at least 300 amino acids, were identified from the Populus genome assembly v1.1 (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html). They were named PtSPL1–PtSPL17, respectively, of which PtSPL3 and PtSPL4 had the highest similarities with AtSPL7 involved in Cu homeostasis . In order to characterize the whole SPL gene family in P. trichocarpa, we searched the Populus genome assembly v1.1, v2.2 and v3.0 . It resulted in the identification of 28 full-length PtSPLs. Gene structures, chromosomal locations, phylogenetic relationships, conserved protein motifs and expression patterns of all identified PtSPLs were systematically analyzed. MiR156-mediated posttranscriptional regulation of PtSPL genes was investigated. The results provide useful information for elucidating the biological functions of SPLs in P. trichocarpa.
Identification of 28 SPL genes in P. trichocarpagenome
PtSPL gene names and gene model IDs in the Populus genome assembly v1.1, v2.2 and v3.0
GRAIL3.0010027501 b + GRAIL3.0010027301b + GRAIL3.0010027401b
ESTEXT_GENEWISE1_V1.C_LG_XIV2145b + GW1.XIV.2149.1b
GRAIL3.0050015101b + GW1.8978.5.1b + GW1.II.489.1b
EUGENE3.00051637b + EUGENE3.00051638b
POPTR_0016s04880b + POPTR_0016s04890b
Estimated age of the duplication events for PtSPL paralogous genes
Estimated time (mya)
PtSPL7 (Chr2)/ PtSPL6 (Chr14)
Phylogenetic analysis of SPLs in P. trichocarpa and Arabidopsis
Comparative analysis of PtSPL and AtSPLgene structures
Gene structure analysis showed that the number of introns in the coding region of 28 PtSPL genes varied from 1 to 10. The number of PtSPLs with 1, 2, 3, 4, 9 and 10 introns is five, ten, four, one, six, and two, respectively (Figure 3, Additional file 1). Similarly, the intron number of 16 AtSPLs varies between 1 and 9 (Additional file 2). The pattern of intron distribution in PtSPLs is quite similar to AtSPLs with the majority to be 2 and 9 introns, followed by 1 and 3 (Figure 3, Additional files 1 and 2) . In addition, the position of intron in the SBP domain is highly conserved. It locates in the codon for the 48th amino acid of SBP domain (Additional file 4). These results suggest the conservation of exon-intron structures between PtSPLs and AtSPLs.
Identification of 25 conserved motifs
E-value and consensus sequences of 25 motifs identified in PtSPLs
Expression patterns of SPLs in P. trichocarpa
MiR156-mediated posttranscriptional regulation of PtSPLs
SPLs are plant-specific transcription factors containing a highly conserved SBP (SQUAMOSA PROMOTER BINDING PROTEIN) domain. It can specifically bind to the promoters of floral meristem identity gene SQUAMOSA and its orthologous genes and plays important regulatory roles in plant growth and development [46–49]. The genes encoding SPLs have been identified from various plant species, such as Arabidopsis[2, 10, 23, 26], maize , Antirrhinum majus, rice , silver birch , and S. miltiorrhiza. SPL genes exist as a large gene family in plants. The number of SPLs in Arabidopsis, rice, P. patens, maize and tomato is 16, 19, 13, 31 and 15, respectively [4–9]. Availability of the whole genome sequence allows us to perform genome-wide identification of SPLs in P. trichocarpa. Analysis of three versions of the annotated P. trichocarpa genome showed the existence of 28 full-length PtSPLs, which distribute on 14 chromosomes. It is the first attempt to analyze the PtSPL gene family. The results provide a basis for elucidating the functions of SPLs in P. trichocarpa, a model forest tree.
The number of SPL genes in P. trichocarpa is much greater than that in Arabidopsis, rice, P. patens and tomato, although it is similar to the number of maize SPLs[4–9]. Sequence homologous analysis suggests that gene duplication plays an important role in SPL gene expansion in P. trichocarpa. A total of 11 pairs of intrachromosome-duplicated PtSPLs were identified in this study. All of them clustered together in the phylogenetic tree (Figure 2). It is consistent with previous findings for generation and maintenance of gene families in other organisms, such as mouse, human and Arabidopsis[52, 53]. Actually, gene duplication has been reported for many plant transcription factor gene families, such as MYB, AP2, MADS and so on [54–56] and duplicated SPL gene pairs have been identified in Arabidopsis (AtSPL10/11, AtSPL4/5 and AtSPL1/12) and rice (OsSPL2/19, OsSPL3/12, OsSPL4/11, OsSPL5/10 and OsSPL16/18) [57–61]. However, the number of homologous PtSPL gene pairs is obviously greater than that in Arabidopsis and rice, indicating that more segment duplication events happened in Populus and most SPL genes in Arabidopsis and Populus expanded in a species-specific manner [62–64].
Comparative analysis of P. trichocarpa PtSPLs and Arabidopsis AtSPLs revealed many conserved sequence features. For instance, all of the deduced proteins contain the highly conserved SBP domain with about 78 amino acid residues. The intron position and intron phase in the SBP-domain-encoding regions are also conserved among all SPL genes in P. trichocarpa and Arabidopsis, indicating that plant SPL genes originate from a common ancestor. Based on the neighbor-joining (NJ) phylogenetic tree constructed using MEGA 5.1., 44 SPL proteins from P. trichocarpa and Arabidopsis were found to cluster into 6 groups. Each group includes at least a PtSPL and one AtSPL. The intron number and intron phase are similar for PtSPLs and AtSPLs within a group. The results suggest the conservation between P. trichocarpa PtSPLs and Arabidopsis AtSPLs.
It has been shown that AtSPLs play significant regulatory roles in a variety of developmental processes in Arabidopsis. For instance, morphological traits of cauline leaves and flowers are regulated by AtSPL2, AtSPL10 and AtSPL11. Juvenile-to-adult growth phase transition and leaf initiation rate are controlled by the redundant action of AtSPL9 and AtSPL15. Pollen sac development, male fertility and GA biosynthesis and signaling are regulated by AtSPL8, a member of G3 [23–25]. Cu homeostasis in Arabidopsis is regulated by the member of group 6, AtSPL7. In this study, we found that many motifs were unique to or mainly existed in a group of SPLs. It is consistent with the redundant roles of AtSPLs in a group and indicates that the members of PtSPLs in the same group may play similar roles as their Arabidopsis counterparts. The function of SPLs in different groups could be functionally distinct. On the other hand, three PtSPL-specific motifs, including motifs 11, 19 and 23, were identified, suggesting that some PtSPLs may play species-specific roles. Consistently, most of paralogous PtSPL gene pairs in the same group show similar expression patterns, whereas a few of them exhibit differential patterns. The results indicate subfunctionalisation and neofunctionalisation of SPLs within a plant species and among different species.
MiR156-medicated posttranscriptional regulation is important for the function of a subset of SPLs[11, 41, 65]. Target prediction showed that all PtSPLs in groups 1, 2 and 5 were regulated by miR156. The complementary sites of miR156 locate in the coding region of G1 and G2 SPLs, whereas it locates in 3’ UTR of G5 SPLs. It is consistent with the results from Arabidopsis SPLs and suggests the conservation of miR156-mediated posttranscriptional regulation in plants.
In this study, a total of 28 full-length SPLs were identified from the whole genome sequence of P. trichocarpa. Through a comprehensive analysis of gene structures, phylogenetic relationships, chromosomal locations, conserved motifs, expression patterns and miR156-mediated posttranscriptional regulation, the PtSPL gene family was characterized and compared with SPLs in Arabidopsis. The results showed that 28 PtSPLs and 16 AtSPLs clustered into 6 groups. Many PtSPLs and AtSPLs within a group are highly conserved in sequence features, gene structures, motifs, expression patterns and posttranscriptional regulation, suggesting the conservation of plant SPLs within a group. However, significant differences were observed for SPLs among groups. In addition, various motifs were identified in PtSPLs but not in AtSPLs. It suggests the diversity of plant SPLs. The results provide useful information for elucidating the functions of SPLs in P. trichocarpa.
Identification of PtSPLgenes
The nucleotide sequences and deduced amino acid sequences of 16 known SPL genes in Arabidopsis[2, 4] were obtained from the TAIR database (http://www.arabidopsis.org) (Additional file 2). The SBP domain of AtSPLs was identified using Pfam (http://pfam.sanger.ac.uk). BLAST search of PtSPLs against Populus trichocarpa v1.1, v2.2 and v3.0 was carried out using AtSPL SBP as the query sequences  (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html,http://www.phytozome.net/poplar.php#B). An e-value cut off of 1e−5 was applied to the recognition. We also searched the databases for SBP using the keywords search tool on the web servers. Protein sequences retrieved from Populus trichocarpa v1.1, v2.2 and v3.0 were then aligned and combined based on sequence identities.
Chromosome location and sequence feature analyses
Chromosome locations of PtSPL genes were determined by BLAST analysis of PtSPLs against Populus trichocarpa v3.0 (http://www.phytozome.net/poplar.php#B). Paralogous gene pairs were analyzed on the Plant Genome Duplication Database (PGDD) server (http://chibba.agtec.uga.edu/duplication/index/locus) with display range for 100 kb. The approximate date of the duplication events was calculated using T = Ks/2λ by assuming clock-like rates (λ) in Populus for 9.0 × 10−9[32, 57, 66]. Synonymous substitutions (Ks) values of paralogous gene pairs were calculated using DnaSP . The theoretical isoelectric point (pI) and molecular weight (Mw) were predicted using the Compute pI/Mw tool on the ExPASy server (http://web.expasy.org/compute_pi/) . The intron/exon structure of SPL genes was predicted with the Gene Structure Display Server (http://gsds.cbi.pku.edu.cn/chinese.php) .
Phylogenetic construction and motif analysis
Phylogenetic trees were constructed using the neighbor-joining (NJ) method in MEGA5.1. Branching reliability was assessed by the bootstrap re-sampling method using 1,000 bootstrap replicates. Only nodes supported by bootstrap values greater than 50% were analyzed. Conserved domains of PtSPLs were identified using Pfam (http://pfam.sanger.ac.uk) and by BLAST analysis of protein sequences against the Conserved Domain Database (CDD, http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) with the expected e-value threshold of 1.0 and the maximum size of hits to be 500 amino acids . The 78 amino acids of SBP domain were aligned using clustalW. Sequence logos were generated using the weblogo platform (http://weblogo.berkeley.edu/). Potential protein motifs were predicted using the MEME package (http://meme.sdsc.edu/meme/) with the following parameters applied. It includes the distribution of motifs: zero and one per sequence, maximum number of motifs to find: 25, minimum width of motif: 8, and maximum width of motif: 150. An e-value cut off of 1e−10 was applied to the recognition.
Quantitative real-time reverse transcription-PCR (qRT-PCR)
P. trichocarpa plants were grown in an artificial climate chamber for about one year. Young leaves (2nd–3rd from the top), mature leaves (12th from the top), young stems (1st–3rd from the top), young roots, tissues of developing secondary xylem and phloem from the 4th–6th and 12th–25th internodes from the top of P. trichocarpa plants were collected. Three biological repeats were carried out. Total RNA was extracted using the plant total RNA extraction kit (Aidlab, China). Genomic DNA contamination was eliminated by pre-treating total RNA with RNase-free DNase (Promega, USA). RNA integrity was analyzed on a 1.2% agarose gel and its quantity was determined using a NanoDrop 2000C Spectrophotometer (Thermo Scientific, USA). Total RNA was reverse-transcribed by Superscript III Reverse Transcriptase (Invitrogen, USA). qRT-PCRs were carried out in triplicate for each tissue sample using gene-specific primers (Additional file 6) as described previously . The program used for qRT-PCR is as follows: predenaturation at 95°C for 30s, 40 cycles of amplification at 95°C for 5 s, 60°C for 18 s and 72°C for 15 s. The length of amplicons was between 80 bp and 250 bp. Actin was used as a reference gene as described previously . Dissociation curve was used to assess amplification specificity. Relative abundance of transcripts was analyzed using the comparative Ct method . The arithmetic formula, 2-ΔΔCq, was used to achieve results for relative quantification. Cq represents the threshold cycle. Standardization of gene expression data from three biological replicates was performed as described . For statistical analysis, ANOVA (analysis of variance) was calculated using SPSS (Version 19.0, IBM, USA). P < 0.05 was considered statistically significant.
Microarray data analysis
Microarray data of PtSPLs was obtained by the ePlant-tissue expression tool at PopGenIE (http://www.popgenie.org/). The data was gene-wise normalized and then analyzed using the average linkage clustering technique in Cluster 3.0 .
Prediction of PtSPLstargeted by miR156
The sequences of P. trichocarpa miR156a–miR156j were obtained from miRBase  (http://www.mirbase.org/). PtSPLs targeted by miR156 were predicted by searching the coding regions and 3’ UTRs of all PtSPLs for complementary sequences of P. trichocarpa miR156a–miR156j on the psRNATarget server using default parameters  (http://plantgrn.noble.org/psRNATarget/?function=3).
Availability of supporting data
The data sets supporting the results of this article are included within the article and its additional files.
The molecular weight
Nuclear location signal
Quantitative realtime reverse transcription-PCR
SQUAMOSA PROMOTER BINDING PROTEIN
Zinc finger 1
Zinc finger 1.
This work was supported by grants from the National Key Basic Research Program of China (973 program) (2012CB114502 to S.L) and the Program for Xiehe Scholars in Chinese Academy of Medical Sciences & Peking Union Medical College (to SL).
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